Bacteriophage S-PM2 infects several strains of the abundant and ecologically important marine cyanobacterium Synechococcus. A large lytic phage with an isometric icosahedral head, S-PM2 has a contractile tail and by this criterion is classified as a myovirus ( Strains of unicellular cyanobacteria of the genera Synechococcus and Prochlorococcus are abundant in the world's oceans and constitute the prokaryotic component of the picophytoplankton. Together, these photosynthetic bacteria contribute a significant proportion of primary production in oligotrophic regions of the oceans (21,35,37,68). Viral infection of marine unicellular cyanobacteria was first reported in 1990 (53, 63), and cyanovirus isolates were first characterized in the laboratory in 1993 (62,69,74). The majority of these phages belong to the myoviruses. Myoviruses are physically robust and remarkably versatile; this virion design can apparently be easily adapted to a variety of different ecological niches (64). S-PM2 is a lytic cyanomyovirus with an icosahedral head and long contractile tail that infects marine Synechococcus strains. The genome has been shown to have a size of ϳ194 kb (27). Bacteriophage T4 that infects Escherichia coli is the archetype myovirus, and S-PM2 was shown to have a genetic module that encodes distant homologues of most of the major virion proteins of T4 (27). T4 has been extensively studied and is extremely well understood; it serves as a superb, if somewhat complex, model for S-PM2.A previous phylogenetic analysis of the sequences of the major head and tail genes of a wide range of T4-type bacteriophages indicated at least three distinct phylogenetic subgroups of these phages (64). There is a large cluster of phages, termed the T-evens, members of which are all closely related to T4, the archetype of the Myoviridae. The second subgroup is surprisingly phylogenetically divergent from the T-evens, but morphologically similar; these are called the pseudoT-evens (47), and they includes phages such as RB49 and RB42 that infect E. coli. The third cluster includes Aeromonas phages and vibriophages such as nt-1, KVP20, KVP40, 65, and Aeh1. Such phages have heads that are more elongated than those of both T-evens and the pseudoT-evens and thus are called the schizoT-evens (64). Phylogenetic analysis based on the major capsid protein gp23 has shown that S-PM2 and the related cyanomyovirus S-PWM3 are quite distinct from the other characterized T4-like phages and form a new discrete group, the exoT-evens (27). These marine T4-type phages have apparently diverged significantly from the T4 archetype. Beyond the fact that they have a contractile tail, these phages have little morphological resemblance to the other T4-type phages. Among the many differences between the exoT-evens and the other T-type phages are those that relate to the photosynthetic physiology of their hosts. It is clear that S-PM2 (41) and several other marine cyanomyoviruses (36, 43) encode homologues of the D1 and D2 proteins of the host photosystem II that presum...
The discovery of the genes psbA and psbD, encoding the D1 and D2 core components of the photosynthetic reaction center PSII (photosystem II), in the genome of the bacteriophage S-PM2 (a cyanomyovirus) that infects marine cyanobacteria begs the question as to how these genes were acquired. In an attempt to answer this question, it was established that the occurrence of the genes is widespread among marine cyanomyovirus isolates and may even extend to podoviruses. The phage psbA genes fall into a clade that includes the psbA genes from their potential Synechococcus and Prochlorococcus hosts, and thus, this phylogenetic analysis provides evidence to support the idea of the acquisition of these genes by horizontal gene transfer from their cyanobacterial hosts. However, the phage psbA genes form distinct subclades within this lineage, which suggests that their acquisition was not very recent. The psbA genes of two phages contain identical 212-bp insertions that exhibit all of the canonical structural features of a group I self-splicing intron. The different patterns of genetic organization of the psbAD region are consistent with the idea that the psbA and psbD genes were acquired more than once by cyanomyoviruses and that their horizontal transfer between phages via a common phage gene pool, as part of mobile genetic modules, may be a continuing process. In addition, genes were discovered encoding a high-light inducible protein and a putative key enzyme of dark metabolism, transaldolase, extending the areas of host-cell metabolism that may be affected by phage infection. Strains of unicellular cyanobacteria Synechococcus and Prochlorococcus are abundant in the world's oceans, and they dominate the prokaryotic component of the picophytoplankton. Together, they contribute 32-89% of primary production in oligotrophic regions of the oceans (1-4). The recent discovery (5) that a phage infecting marine Synechococcus strains encodes key photosynthetic genes has important implications for our understanding of the effect of phage infection on the photosynthetic picophytoplankton physiology and consequent impact on major biogeochemical cycles. The acquisition of photosynthesis genes by a phage, presumably by horizontal gene transfer, begs the questions of (i) how common the possession of photosynthesis genes by such phages is, (ii) where the acquired genes were from, and (iii) whether the acquisition was a single rare ancestral event or a common phenomenon in the oceans.The cyanobacterial picoplankton, together with all organisms capable of oxygenic photosynthesis, possess two photosynthetic reaction centers, PSI and PSII (photosystems I and II). The PSII complex is a large protein-pigment assembly in the thylakoid membrane that catalyses the light-dependent oxidation of water to molecular oxygen. At the core of PSII lies a heterodimer of two related proteins, D1 and D2, which binds the pigments and cofactors necessary for primary photochemistry. During active photosynthesis, D1 and, to a lesser extent, D2 turn over rapidly as...
Unicellular cyanobacteria of the genus Synechococcus are a major component of the picophytoplankton and make a substantial contribution to primary productivity in the oceans. Here we provide evidence that supports the hypothesis that virus infection can play an important role in determining the success of different Synechococcus genotypes and hence of seasonal succession. In a study of the oligotrophic Gulf of Aqaba, Red Sea, we show a succession of Synechococcus genotypes over an annual cycle. There were large changes in the genetic diversity of Synechococcus, as determined by restriction fragment length polymorphism analysis of a 403- bp rpoC1 gene fragment, which was reduced to one dominant genotype in July. The abundance of co-occurring cyanophage capable of infecting marine Synechococcus was determined by plaque assays and their genetic diversity was determined by denaturing gradient gel electrophoresis analysis of a 118-bp g20 gene fragment. The results indicate that both abundance and genetic diversity of cyanophage covaried with that of Synechococcus. Multivariate statistical analyses show a significant relationship between cyanophage assemblage structure and that of Synechococcus. These observations are consistent with cyanophage infection being a major controlling factor in picophytoplankton succession.
The vast majority of cyanophages isolated to date are cyanomyoviruses, a group related to bacteriophage T4. Comparative genome analysis of five cyanomyoviruses, including a newly sequenced cyanophage S-RSM4, revealed a 'core genome' of 64 genes, the majority of which are also found in other T4-like phages. Subsequent comparative genomic hybridization analysis using a pilot microarray showed that a number of 'host' genes are widespread in cyanomyovirus isolates. Furthermore, a hyperplastic region was identified between genes g15-g18, within a highly conserved structural gene module, which contained a variable number of inserted genes that lacked conservation in gene order. Several of these inserted genes were host-like and included ptoX, gnd, zwf and petE encoding plastoquinol terminal oxidase, 6-phosphogluconate dehydrogenase, glucose 6-phosphate dehydrogenase and plastocyanin respectively. Phylogenetic analyses suggest that these genes were acquired independently of each other, even though they have become localized within the same genomic region. This hyperplastic region contains no detectable sequence features that might be mechanistically involved with the acquisition of host-like genes, but does appear to be a site specifically associated with the acquisition process and may represent a novel facet of the evolution of marine cyanomyoviruses.
The bacterial SeqA protein binds to hemi-methylated GATC sequences that arise in newly synthesized DNA upon passage of the replication machinery. In Escherichia coli K-12, the single replication origin oriC is a well-characterized target for SeqA, which binds to multiple hemi-methylated GATC sequences immediately after replication has initiated. This sequesters oriC, thereby preventing reinitiation of replication. However, the genome-wide DNA binding properties of SeqA are unknown, and hence, here, we describe a study of the binding of SeqA across the entire Escherichia coli K-12 chromosome, using chromatin immunoprecipitation in combination with DNA microarrays. Our data show that SeqA binding correlates with the frequency and spacing of GATC sequences across the entire genome. Less SeqA is found in highly transcribed regions, as well as in the ter macrodomain. Using synchronized cultures, we show that SeqA distribution differs with the cell cycle. SeqA remains bound to some targets after replication has ceased, and these targets locate to genes encoding factors involved in nucleotide metabolism, chromosome replication, and methyl transfer.
From genomic sequencing it has become apparent that the marine cyanomyoviruses capable of infecting strains of unicellular cyanobacteria assigned to the genera Synechococcus and Prochlorococcus are not only morphologically similar to T4, but are also genetically related, typically sharing some 40-48 genes. The large majority of these common genes are the same in all marine cyanomyoviruses so far characterized. Given the fundamental physiological differences between marine unicellular cyanobacteria and heterotrophic hosts of T4-like phages it is not surprising that the study of cyanomyoviruses has revealed novel and fascinating facets of the phage-host relationship. One of the most interesting features of the marine cyanomyoviruses is their possession of a number of genes that are clearly of host origin such as those involved in photosynthesis, like the psbA gene that encodes a core component of the photosystem II reaction centre. Other host-derived genes encode enzymes involved in carbon metabolism, phosphate acquisition and ppGpp metabolism. The impact of these host-derived genes on phage fitness has still largely to be assessed and represents one of the most important topics in the study of this group of T4-like phages in the laboratory. However, these phages are also of considerable environmental significance by virtue of their impact on key contributors to oceanic primary production and the true extent and nature of this impact has still to be accurately assessed.
Summary Bacteriophages infecting Escherichia coli (coliphages) have been used as a proxy for faecal matter and water quality from a variety of environments. However, the diversity of coliphages that is present in seawater remains largely unknown, with previous studies largely focusing on morphological diversity. Here, we isolated and characterized coliphages from three coastal locations in the United Kingdom and Poland. Comparative genomics and phylogenetic analysis of phage isolates facilitated the identification of putative new species within the genera Rb69virus and T5virus and a putative new genus within the subfamily Tunavirinae. Furthermore, genomic and proteomic analysis combined with host range analysis allowed the identification of a putative tail fibre that is likely responsible for the observed differences in host range of phages vB_Eco_mar003J3 and vB_Eco_mar004NP2.
The aim of this study was to determine the abundance of cyanophages over an annual cycle in the Red Sea from the period April 1999 to December 1999 at a range of depths. Cyanophage numbers from 71 water samples were determined by the use of plaque assays using four di¡erent Synechococcus strains. The results indicate that cyanophage are found throughout the water column from surface waters to depths of 150 m, with a discrete maximum in the number of cyanophages in the summer months of July, August and September at a depth of 30 m. Eighty-seven cyanophages were isolated and characterized in terms of host range, genome size and possession of a myoviral portal vertex gene. Cyanophages were found to infect multiple strains of Synechococcus from di¡erent phylogenetic clades. The genome sizes of cyanophages were also found to be bigger than previously estimated.
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